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Epidemiology
Original research
Impacts of armed conflicts on tuberculosis burden and treatment outcomes: a systematic review
  1. Eyob Alemayehu Gebreyohannes1,2,3,
  2. Haileab Fekadu Wolde1,4,
  3. Temesgen Yihunie Akalu1,4,5,
  4. Archie C A Clements1,6,
  5. Kefyalew Addis Alene1,4
  1. 1Geospatial and Tuberculosis Research Team, Telethon Kids Institute, Perth, Western Australia, Australia
  2. 2School of Allied Health, The University of Western Australia, Perth, Western Australia, Australia
  3. 3Quality Use of Medicines and Pharmacy Research Centre, Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia
  4. 4School of Population Health, Faculty of Health Sciences, Curtin University, Perth, Western Australia, Australia
  5. 5Institute of Public Health, College of Medicine and Health Sciences, University of Gondar, Gondar, Amhara, Ethiopia
  6. 6Penninsula Medical School, University of Plymouth, Playmouth, UK
  1. Correspondence to Dr Eyob Alemayehu Gebreyohannes; justeyob{at}gmail.com

Abstract

Objectives This systematic review aimed to summarise existing literature on the impacts of armed conflicts on tuberculosis burden and treatment outcomes.

Design A systematic review following the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses guidelines.

Data sources PubMed, Web of Science, Cumulative Index to Nursing and Allied Health Literature Plus, Scopus, ScienceDirect, Embase and medRxiv.

Data extraction and synthesis Three reviewers independently screened, selected eligible studies and extracted data. A narrative review was undertaken to summarise the findings qualitatively.

Results Eleven studies were included in this review, reporting on tuberculosis incidence rates, prevalence and treatment outcomes, including mortality. Overall, the impact of armed conflicts on case notifications was variable. Six studies reported overall increases in tuberculosis case notifications following the onset of conflicts, while three studies reported overall decreases in tuberculosis case notifications. Factors, including limited access to healthcare services, challenges in surveillance and laboratory confirmation, the destruction of health systems and incapacitating the healthcare workforce, contributed to a decrease in the number of notified cases. The higher tuberculosis notification in some of the studies could be attributed to the disruption of tuberculosis prevention and control programmes as well as increased socioeconomic deprivation, including malnutrition, mass migration, poor living conditions and overcrowding that are worsened during conflicts. Armed conflicts without effective interventions were associated with worse tuberculosis treatment outcomes, including lower proportions of people with treatment success and higher proportions of people with loss to follow-up, mortality and treatment failure. However, implementing various interventions in conflict settings (such as establishing a National Tuberculosis Control Programme) led to higher tuberculosis notification rates and treatment success.

Conclusion The impact of armed conflicts on tuberculosis notification is complex and is influenced by multiple factors. The findings of this review underscore the importance of concerted efforts to control tuberculosis in conflict settings using available resources.

  • tuberculosis
  • epidemiology
  • public health

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information.

http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/bmjopen-2023-080978

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    STRENGTHS AND LIMITATIONS OF THIS STUDY

    • This systematic review employed a thorough search across multiple databases, including a preprint database, contributing to a comprehensive synthesis of available evidence.

    • Key elements such as the severity of armed conflicts in each study were not evaluated, posing potential confounding factors.

    • The review’s dependence on studies explicitly mentioning armed conflicts may have resulted in the oversight of studies conducted in regions and timeframes of armed conflicts that did not make explicit references to the conflict.

    Introduction

    Tuberculosis (TB) is one of the most important public health problems globally. It was responsible for the deaths of an estimated 1.3 million people worldwide in 2022, making it the second leading cause of mortality from a single infectious agent, only second to COVID-19.1 TB disproportionately affects people in low-income and middle-income countries (LMICs), especially countries in the WHO Africa and South-East Asia regions,1 which, in 2022, accounted for 81% of all TB deaths globally.1 These are also regions where armed conflicts frequently occur.2 However, there are examples of countries with a high burden of TB within all income level groups and all WHO regions. Armed conflicts are not just confined to LMICs, as the ongoing Russo-Ukrainian and Israel-Hamas armed conflicts show. Notably, Russia and Ukraine are both countries with a significant burden of TB and a high incidence of drug-resistant TB,1 and the refugee crisis created by the conflict can potentially increase TB transmission throughout Europe and other destinations for displaced people.3 4

    Armed conflicts refer to confrontations between regular or irregular armed groups with the continuous and organised use of violence.2 In 2021, a total of 32 armed conflicts were reported, mostly from LMICs in Africa and Asia.2 These conflicts were responsible for the loss of an estimated 150 000 lives in 2021.5 In addition to conflicts between nations, non-state conflicts and internationalised intrastate conflicts continue to pose significant challenges to achieving sustainable peace in the world.6

    Armed conflicts contribute to the spread of infectious diseases such as TB by destroying existing healthcare systems, disrupting prevention programmes, destroying infrastructure and worsening housing, sanitation and hygiene.7 In addition, overcrowding and malnutrition contribute to the increase in the burden of TB during armed conflicts.8 Armed conflicts can also be responsible for driving the spread of infectious diseases to non-conflict-affected areas due to the displacement of people.7 Considering the ongoing armed conflicts and the current geopolitical landscape, it is important to review existing evidence on the scale of the impact of armed conflict on TB burden and treatment outcomes to better inform governments and international organisations of the additional resourcing required to mitigate the impact and to inform a broader perspective on the cost of conflict beyond the estimation of direct casualties. Therefore, this review aims to summarise the existing literature on the impacts of armed conflicts on TB burden and treatment outcomes globally.

    Methods

    Search strategy

    We followed the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses guidelines for reporting standards.9 Six electronic databases (PubMed, Web of Science, Cumulative Index to Nursing and Allied Health Literature Plus, Scopus, ScienceDirect and Embase) were searched from 2000 to 16 August 2022, along with the medRxiv database for preprints. While there are several older studies, particularly those focused on the two World Wars, we were interested in the past two decades (2000–2022). Only studies conducted on humans were included without any language restrictions. The key search terms used were ‘tuberculosis’, ‘armed conflict’ and ‘war’. The detailed search strategy for all databases is presented in online supplemental table 1. The protocol for this systematic review is published at PROSPERO (CRD42022354382).

    Study eligibility

    Studies that assessed the impact of armed conflicts on TB burden (ie, prevalence and incidence) or treatment outcomes were eligible for inclusion. To be included, studies must have compared TB burdens in prearmed and postarmed conflict periods. Alternatively, studies may have compared areas of armed conflict with similar areas that did not have armed conflict. Studies must have assessed incidence rates (including case notification rates), prevalence of TB, mortality rate associated with TB, TB treatment outcomes10 (treatment success (cure and treatment completion) and poor treatment outcomes (treatment failure, death and loss to follow-up)) or medication adherence for TB. Studies solely focused on refugees or migrants were excluded, as previous systematic reviews have already addressed those populations.11 12 Other reasons for exclusion are shown in online supplemental table 2.

    Data extraction

    Three reviewers (EAG, HFW and TYA) independently screened (based on title and abstract), selected eligible studies (after full-text review) and extracted data. Screening and data extraction for each study were conducted by at least two reviewers. Discrepancies were resolved through consensus and discussion with a third reviewer.

    The following data were extracted from the included studies: bibliographic details (name of the first author, year of publication and journal), country where the study was conducted, study design, study setting, population, start and end years of the conflict, type of TB, outcome measures, population size in the study area, number of TB cases and TB-related deaths in the study area, type of TB treatment, number of patients taking TB treatment and treatment outcomes.

    Quality assessment

    Two authors (TYA and HFW) independently evaluated the methodological quality of the included primary studies using the Newcastle Ottawa Scale.13 14

    Data analysis

    We used a narrative data synthesis to summarise the findings. We did not perform a meta-analysis due to significant heterogeneity across the included studies. The impact of armed conflict on the outcome of interest was assessed either before and after the onset of armed conflicts or between conflict-affected and non-affected geographic areas. The main outcomes of interest included TB frequency (ie, case notification, prevalence and incidence rate) and TB treatment outcomes (ie, cure, treatment completed, failure, death and loss to follow-up). TB treatment outcomes were classified as ‘treatment success’ when studies report cure and/or treatment completion and as ‘poor treatment outcomes’ when studies report treatment failure, death and/or loss to follow-up. We considered treatment outcomes to have improved if there was an increase in the proportion of people with treatment success and/or a decrease in the proportion of people with poor treatment outcomes after the onset of the conflicts, as compared with the preconflict period. Conversely, treatment outcomes were deemed to have worsened if there was a decrease in the proportions of people with treatment success and/or an increase in the proportions of people with poor treatment outcomes after the start of conflicts compared with the preconflict periods. We synthesised the results under two headings: ‘the impact of armed conflict on TB frequency’ and ‘the impact of armed conflict on TB treatment outcomes’.

    Patient and public involvement

    None.

    Results

    Study selection

    A total of 8254 studies, including 2463 preprints, were retrieved from the seven electronic databases. After removing duplicates and subsequent title and abstract screening, 69 studies were selected for full-text screening. Finally, 11 studies fulfilling the eligibility criteria were included in the systematic review (figure 1).

    Figure 1
    Figure 1

    Flow chart depicting the study selection process.

    Characteristics of the included studies

    The characteristics of the included studies are shown in table 1. The included studies were published between 2000 and 2020.15–25 While 10 of the studies were based on data from a single country, one study18 reported findings from 16 countries. Two of the studies assessed outcomes between conflict-affected areas compared with areas that did not have conflict.21 25 The remaining nine studies assessed outcomes in the same areas by comparing before and after the onset of armed conflicts (table 1). The included studies reported on TB incidence rates, prevalence of TB, mortality rates associated with TB and TB treatment outcomes. None of the included studies reported on adherence to TB medications. Most of the included studies were solely (n=7) or partly (n=8) conducted in the WHO African region. Five,18–21 24 four16 17 23 25 and one22 of the included studies were judged to have good, fair and poor methodological quality, respectively. We did not assess the methodological quality of the included scoping review.15

    View this table:
    Table 1

    Characteristics of the studies that assessed the impact of armed conflicts on tuberculosis burden and treatment outcomes

    The impact of armed conflict on TB frequency

    Nine studies assessed the impact of armed conflicts on TB case notification, prevalence and incidence.15–18 21–25 Overall, the impact of armed conflicts on case notifications was variable (table 2).

    View this table:
    Table 2

    The impact of armed conflict on TB notification

    Six studies reported overall increases in TB case notifications after the start of the conflict in contrast to the preconflict period.16 18 22–25 The first study compared TB notification 3 years after the outbreak of a conflict relative to 3 years before the onset of the conflict in 16 countries.18 Overall, TB notification showed a 10% increase in conflict times (351 307) compared with preconflict times (317 614). However, this was not consistent across all countries. TB notification increased postconflict for half of the 16 countries and decreased for the other half (figure 2). Among the five remaining studies that documented overall increases in TB case notifications, three (specifically, studies conducted in Afghanistan, East Timor and Nigeria) reported the implementation of different interventions during the conflict periods.16 23 24 These included a rapid expansion of the direct observed treatment short course (DOTS) strategy, the establishment of a National TB Control Programme and interventions that aimed to increase case finding. The study from Côte d'Ivoire revealed that TB notifications increased overall in both conflict-affected and unaffected areas following the start of the conflict, compared with the year before the conflict began. However, the increase in median number of TB cases per year was greater in conflict-affected areas (which saw a 16.85% increase from the baseline) compared with areas not affected by the conflict (which saw an 11.14% increase).25 The higher TB notification in some of the studies could be attributed to the disruption of TB prevention and control programmes, malnutrition, mass migration, poor living conditions and overcrowding.22 24 25

    Figure 2
    Figure 2

    Three-year postconflict versus 3-year preconflict per cent change in TB notification by country as reported by Drobniewski and Verlander (2000).18 All indicates the per cent change in all countries collectively. TB, tuberculosis.

    Three studies reported overall decreases in TB case notifications in areas or time periods with conflict in contrast to areas or time periods with no conflict.15 17 21 They also identified several factors that may have influenced TB case notifications, including restricted access to healthcare caused by armed conflicts, challenges related to surveillance and laboratory confirmation, the destruction of health systems and incapacitating the healthcare workforce.15 17 21 The first study, a study from Sudan, compared TB notification in the conflict-affected Darfur region relative to Eastern Sudan, where there had been no conflicts at the time of publication.21 Over a period of 11 years (2004–2014), notification rates were lower in the conflict zone (37 and three cases per 100 000 population for new and retreatment cases, respectively) compared with the non-conflict zone (88 and 4.5 per 100 000 population for new and retreatment cases, respectively). In a study from Syria, TB incidence was 23 cases per 100 000 prior to the onset of the conflict (2010).15 This figure remained the same after 2 years (2012) and showed a slight reduction to 19 cases per 100 000 after 7 years (2017). Lastly, in a study from Liberia, the median number of notified TB cases per year more than doubled after the end of the conflict compared with the conflict period (2523 vs 5486).17 Average TB prevalence was 0.40% (1990, 1995 and 2000) for the conflict period and 0.46% (2005, 2009–2013) for the postconflict period.

    The impact of armed conflict on TB treatment outcomes

    Nine studies assessed the impact of armed conflicts on TB treatment outcomes.16 17 19–25 Six of these studies16 17 21–23 25 assessed treatment success, and seven16 19–24 studies assessed different forms of poor treatment outcomes. While four studies16 21 23 24 reported overall improvements in TB treatment outcomes (ie, increase or decrease in the proportions of people with treatment success and/or poor treatment outcomes, respectively) after the start of conflicts in comparison to the preconflict periods, the remaining five studies17 19 20 22 25 reported worse treatment outcomes. Notably, two of these five studies originated in Guinea-Bissau and addressed the same armed conflict19 20 (table 3). Three of the four studies that reported overall improvements during the conflict-affected periods involved different interventions, as described above.16 23 24

    View this table:
    Table 3

    The impact of armed conflict on tuberculosis treatment outcomes

    Discussion

    This comprehensive, systematic review presents the global impacts of armed conflict on TB burden and treatment outcomes. The findings of the review showed that armed conflicts can lead to mixed results with respect to TB notifications and treatment outcomes, depending on the availability of relief efforts and supportive interventions, and the impact of the conflict on the TB notification system. These findings indicate that while armed conflict adversely affects TB control programmes in most studies, the relationship is complex. Some scholars refer to the post-World War II period we live in as ‘the long peace’, citing fewer large interstate wars as a justification.26 However, millions of people have died due to armed conflicts since 1945,26 27 with almost constant conflicts occurring in different hotspots around the world, right through to the current time.2 6 In 2022, the number of armed conflicts experienced a marginal uptick in comparison to the preceding year. A total of 33 incidents were documented, contrasting with 32 conflicts in 2021 and 34 in each of the years 2020, 2019 and 2018.28

    The impact of armed conflicts on TB notification involves complex processes in which the net effect varies. Localised armed conflicts may have a minimal negative impact on TB notification unless healthcare services are disrupted.18 Underdiagnosis and underreporting can result from the destruction of diagnostic health facilities and surveillance programmes, leading to a reduction in the number of notified TB cases.7 Moreover, the documented destruction of electricity power plants and the resulting power interruptions in times of armed conflicts may exacerbate challenges to the efficacy of TB surveillance endeavours, particularly those reliant on electronic filing systems.29 Our systematic review highlights that limited access to healthcare due to armed conflicts,21 difficulties with surveillance and laboratory confirmation,15 the destruction of health systems, including National TB Control Programmes,17 and killing or otherwise incapacitating healthcare workers17 were some of the reasons that contributed to the lower number of notified cases in some studies. Furthermore, due to the latency of TB,30 the increase in TB transmission during conflicts may increase notifications at a later date rather than immediately. This may lead to an initial decline in TB notifications.

    On the other hand, the TB burden may increase during or after armed conflicts due to conflict-associated risk factors such as the disruption of TB prevention and control programmes, malnutrition, poor sanitation and hygiene and mass migration of people to relatively safer areas, leading to poor living conditions and overcrowding.7 8 22 24 25 These factors may facilitate TB transmission in the affected community and increase the risk of progression from latent to active TB. The intensity of armed conflicts also plays a role in the number of notified TB cases. For example, though there was an overall increase in the number of notified TB cases in Adamawa State in Nigeria, TB notifications increased or decreased in areas where the intensity of armed conflicts was low or high, respectively.24 According to Pembi et al, displacement of the population and a lack of health services lead to a decline in the number of notified TB cases in areas of high-intensity conflict. By contrast, areas of low-intensity conflict had a higher number of notified TB cases due to minimal disruptions to healthcare services and population migration from high-conflict areas, with widespread malnutrition and overcrowding in the displaced population.

    When it comes to treatment outcomes, armed conflict seems to lead to worse outcomes for patients treated for TB. Our review found that, in the absence of effective interventions, armed conflicts are associated with lower proportions of treatment success and/or higher proportions of poor treatment outcomes.17 19 20 22 25 Most of the factors that affected TB notification also contributed to worse treatment outcomes. These include system-level and individual-level factors such as weakened healthcare systems, a lack of healthcare workers, malnutrition, a higher burden of comorbidities such as HIV infection, a lack of TB medications and treatment interruption.17 19 20 Documented disruptions in the supply chain of life-saving anti-TB medications have tragically led to the loss of lives in conflict-affected regions.15 31 Additionally, reports indicate that the destruction of electricity and power infrastructures and hospitals could further compound the challenges and adversely impact the treatment outcomes of hospitalised patients with TB.29

    This review also identified encouraging findings on the impact of TB control interventions in some conflict environments. For instance, the Rural Expansion of Afghanistan’s Community-based Healthcare Programme in Afghanistan successfully implemented a rapid expansion of the DOTS strategy. This led to effective case detection, referrals and home-based DOTS leading to higher TB notification rates despite the destruction of the National TB Programme and basic health services. It also led to higher proportions of treatment success despite the armed conflicts.16 Similarly, the establishment of a National TB Control Programme during an armed conflict in East Timor led to higher TB notification rates and proportions of treatment success and lower proportions of poor treatment outcomes.23 The study from Nigeria also reported that the increase in the number of notified TB cases coincided with the implementation of an intervention that aimed to increase case finding and the introduction of GeneXpert testing. The intervention included health education, the deployment of community volunteers and retraining of health workers in the identification, diagnosis and treatment of TB. This probably also contributed to the small reduction in the proportion of people with poor treatment outcomes during the conflict.24 The above findings suggest that despite the challenges posed by armed conflicts, TB control interventions can be successfully implemented to improve case detection, referrals and treatment outcomes for affected populations. It highlights the importance of continued investment in TB control programmes, even in conflict-affected areas.

    This review has some limitations. First, the time periods to assess the effect of armed conflicts on TB notification and treatment outcomes varied, making it difficult to make direct comparisons between studies. Second, important confounders, including the intensity of armed conflicts in each study, were not assessed. We also relied on studies that made specific reference to armed conflicts and studies that were conducted in areas and periods of armed conflicts but that did not refer to the conflict that may have been missed. Lastly, because there were not enough studies, we did not differentiate the impact of armed conflicts on short-term and long-term outcomes.

    Conclusion

    Armed conflicts have a complex impact on TB notification, influenced by factors like limited healthcare access, challenges in surveillance and laboratory confirmation, the destruction of health systems and incapacitating the healthcare workforce, resulting in a decreased number of notified cases. Conversely, disruptions in TB control programmes, malnutrition and mass migration to safer areas can lead to increased TB notification rates. Furthermore, armed conflicts without effective interventions are associated with worse treatment outcomes, including lower proportions of treatment success and higher proportions of poor treatment outcomes. Lastly, the implementation of various interventions in conflict environments can lead to an increase in rates of TB notification and proportions of treatment success. Therefore, it is crucial to develop and implement effective interventions to sustain and enhance TB control efforts in conflict environments.

    Data availability statement

    All data relevant to the study are included in the article or uploaded as supplementary information.

    Ethics statements

    Patient consent for publication

    Ethics approval

    Not applicable.

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    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    Footnotes

    • Contributors EAG, HFW, TYA, ACAC and KAA contributed to the concept, design and scope of this review. EAG, HFW and TYA contributed to screening, data extraction and study quality assessment. EAG conducted data synthesis and wrote the first draft of the manuscript. EAG was responsible for the overall content as the guarantor. All authors critically reviewed, edited and approved the final manuscript.

    • Funding KAA is funded by an Australian National Health and Medical Research Council Investigator Grant (# APP1196549).

    • Competing interests None declared.

    • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.